Browse > Article
http://dx.doi.org/10.5423/PPJ.OA.07.2020.0121

Antagonistic Activity of Bacteria Isolated from Apple in Different Fruit Development Stages against Blue Mold Caused by Penicillium expansum  

Lopez-Gonzalez, Rocio Crystabel (Division de Estudios de Posgrado, Facultad de Quimica, Universidad Autonoma de Queretaro)
Juarez-Campusano, Yara Suhan (Division de Estudios de Posgrado, Facultad de Quimica, Universidad Autonoma de Queretaro)
Rodriguez-Chavez, Jose Luis (Division de Estudios de Posgrado, Facultad de Quimica, Universidad Autonoma de Queretaro)
Delgado-Lamas, Guillermo (Instituto de Quimica, Universidad Nacional Autonoma de Mexico)
Medrano, Sofia Maria Arvizu (Division de Estudios de Posgrado, Facultad de Quimica, Universidad Autonoma de Queretaro)
Martinez-Peniche, Ramon Alvar (Division de Estudios de Posgrado, Facultad de Quimica, Universidad Autonoma de Queretaro)
Pacheco-Aguilar, Juan Ramiro (Division de Estudios de Posgrado, Facultad de Quimica, Universidad Autonoma de Queretaro)
Publication Information
The Plant Pathology Journal / v.37, no.1, 2021 , pp. 24-35 More about this Journal
Abstract
Blue mold caused by Penicillium expansum is one of the most significant postharvest diseases of apples. Some microorganisms associated with the surface of ripening apples possess the ability to inhibit the growth of P. expansum. However, the existing literature about their colonization in the stages before ripening is not explored in depth. This study aims to characterize the antagonistic capacity of bacterial populations from five fruit development stages of 'Royal Gala' apples. The results have shown that the density of the bacterial populations decreases throughout the ripening stages of fruit (from 1.0 × 105 to 1.1 × 101 cfu/㎠). A total of 25 bacterial morphotypes (corresponding to five genera identified by 16S RNA) were differentiated in which Bacillus stood out as a predominant genus. In the in vitro antagonism tests, 10 Bacillus strains (40%) inhibited the mycelial growth of P. expansum from 30.1% to 60.1%, while in fruit bioassays, the same strains reduced the fruit rot ranging from 12% to 66%. Moreover, the bacterial strains with antagonistic activity increased in the ripening fruit stage. B. subtilis subsp. spiziennii M24 obtained the highest antagonistic activity (66.9% of rot reduction). The matrix-assisted laser desorption ionization-time of flight mass spectrometry analysis revealed that bacteria with antagonistic activity produce anti-fungal lipopeptides from iturin and fengycin families.
Keywords
antifungal activity; Bacillus spp.; epiphyte; fengycin; relative abundance;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 Teixido, N., Usall, J., Magan, N. and Vinas, I. 1999. Microbial population dynamics on Golden Delicious apples from bud to harvest and effect of fungicide applications. Ann. Appl. Biol. 134:109-116.   DOI
2 Tessmer, M. A., Appezzato-da-Gloria, B. and Antoniolli, L. R. 2016. Influence of growing sites and physicochemical features on the incidence of lenticel breakdown in 'Gala' and 'Galaxy' apples. Sci. Hortic. 205:119-126.   DOI
3 The R Foundation. 2020. The R project for statistical computing. URL https://www.r-project.org/ [14 July 2020].
4 Tosco, A., Chobelet, A., Bathany, K., Schmitter, J.-M., Urdaci, M. C. and Bure, C. 2015. Characterization by tandem mass spectrometry of biologically active compounds produced by Bacillus strains. J. Appl. Bioanal. 1:19-25.   DOI
5 Venables, W. N. and Ripley, B. D. 2002. Modern applied statistics with S. 4th ed.Springer, New York, NY, USA. 495 pp.
6 Wallace, R. L., Hirkala, D. L. and Nelson, L. M. 2017. Postharvest biological control of blue mold of apple by Pseudomonas fluorescens during commercial storage and potential modes of action. Postharvest Biol. Technol. 133:1-11.   DOI
7 Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., Szoecs, E. and Wagner, H. 2015. vegan: community ecology package: ordination methods, diversity analysis and other functions for community and vegetation ecologists. R package, version 2.5-6. URL https://cran.r-project.org/src/contrib/Archive/vegan/ [14 July 2020].
8 R Core Team. 2013. R: A language and environment for statistical computing. URL http://www.R-project.org/ [14 July 2020].
9 Rodriguez-Chavez, J. L., Juarez-Campusano, Y. S., Delgado, G. and Pacheco Aguilar, J. R. 2019. Identification of lipopeptides from Bacillus strain Q11 with ability to inhibit the germination of Penicillium expansum, the etiological agent of postharvest blue mold disease. Postharvest Biol. Technol. 155:72-79.   DOI
10 Rudrappa, T., Czymmek, K. J., Pare, P. W. and Bais, H. P. 2008. Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol. 148:1547-1556.   DOI
11 Rungjindamai, N. 2016. Isolation and evaluation of biocontrol agents in controlling anthracnose disease of mango in Thailand. J. Plant Prot. Res. 56:306-311.   DOI
12 Saravanakumar, D., Ciavorella, A., Spadaro, D., Garibaldi, A. and Gullino, M. L. 2008. Metschnikowia pulcherrima strain MACH1 outcompetes Botrytis cinerea, Alternaria alternata and Penicillium expansum in apples through iron depletion. Postharvest Biol. Technol. 49:121-128.   DOI
13 Sartori, M., Nesci, A., Formento, A. and Etcheverry, M. 2015. Selection of potential biological control of Exserohilum turcicum with epiphytic microorganisms from maize. Rev. Argent. Microbiol. 47:62-71.   DOI
14 Droby, S. and Wisniewski, M. 2018. The fruit microbiome: a new frontier for postharvest biocontrol and postharvest biology. Postharvest Biol. Technol. 140:107-112.   DOI
15 Sarwar, A., Brader, G., Corretto, E., Aleti, G., Ullah, M. A., Sessitsch, A. and Hafeez, F. Y. 2018. Qualitative analysis of biosurfactants from Bacillus species exhibiting antifungal activity. PLoS ONE 13:e0198107.   DOI
16 Konarska, A. 2014. Morphological, histological and ultrastructural changes in fruit epidermis of apple Malus domestica cv. Ligol (Rosaceae) at fruit set, maturity and storage. Acta Biol. Crac. Ser. Bot. 56:35-48.
17 Krzyzanowska, D. M., Maciag, T., Siwinska, J., Krychowiak, M., Jafra, S. and Czajkowski, R. 2019. Compatible mixture of bacterial antagonists developed to protect potato tubers from soft rot caused by Pectobacterium spp. and Dickeya spp. Plant Dis. 103:1374-1382.   DOI
18 Leff, J. W. and Fierer, N. 2013. Bacterial communities associated with the surfaces of fresh fruits and vegetables. PLoS ONE 8:e59310.   DOI
19 Anderson, M. J. 2008. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26:32-46.   DOI
20 Arrebola, E., Sivakumar, D., Bacigalupo, R. and Korsten, L. 2010. Combined application of antagonist Bacillus amyloliquefaciens and essential oils for the control of peach postharvest diseases. Crop Prot. 29:369-377.   DOI
21 Dukare, A. S., Paul, S., Nambi, V. E., Gupta, R. K., Singh, R., Sharma, K. and Vishwakarma, R. K. 2019. Exploitation of microbial antagonists for the control of postharvest diseases of fruits: a review. Crit. Rev. Food Sci. Nutr. 59:1498-1513.   DOI
22 Fediala Abd El-Gleel Mosa, W., Sas Paszt, L., Frac, M., Trzcinski, P., Treder, W. and Klamkowski, K. 2018. The role of biofertilizers in improving vegetative growth, yield and fruit quality of apple. Hortic. Sci. (Prague) 45:173-180.   DOI
23 Fourie, J. F. and Holz, G. 1998. Effects of fruit and pollen exudates on growth of Botrytis cinerea and infection of plum and nectarine fruit. Plant Dis. 82:165-170.   DOI
24 Fredriksson, N. J., Hermansson, M. and Wilen, B. M. 2013. The choice of PCR primers has great impact on assessments of bacterial community diversity and dynamics in a wastewater treatment plant. PLoS ONE 8:e76431.   DOI
25 Lopes, P. R. C., Oliveira, I. V. D. M., Silva, R. R. S. D. and Cavalcante, Í. H. L. 2013. Growing Princesa apples under semiarid conditions in northeastern Brazil. Acta Sci. Agron. 35:93-99.
26 Leibinger, W., Breuker, B., Hahn, M. and Mendgen, K. 1997. Control of postharvest pathogens and colonization of the apple surface by antagonistic microorganisms in the field. Phytopathology 87:1103-1110.   DOI
27 Li, H. X. and Xiao, C. L. 2008. Characterization of fludioxonil-resistant and pyrimethanil-resistant phenotypes of Penicillium expansum from apple. Phytopathology 98:427-435.   DOI
28 Li, Y., Han, L.-R., Zhang, Y., Fu, X., Chen, X., Zhang, L., Mei, R. and Wang, Q. 2013. Biological control of apple ring rot on fruit by Bacillus amyloliquefaciens 9001. Plant Pathol. J. 29:168-173.   DOI
29 Lorenzini, M. and Zapparoli, G. 2020. Epiphytic bacteria from withered grapes and their antagonistic effects on grape-rotting fungi. Int. J. Food Microbiol. 319:108505.   DOI
30 Luziatelli, F., Ficca, A. G., Colla, G., Baldassarre Svecova, E. and Ruzzi, M. 2019. Foliar application of vegetal-derived bioactive compounds stihhajeo mulates the growth of beneficial bacteria and enhances microbiome biodiversity in lettuce. Front. Plant Sci. 10:60.   DOI
31 Shehata, M. G., Badr, A. N., Abdel-Razek, A. G., Hassanein, M. M. and Amra, H. A. 2017. Oil-bioactive films as an antifungal application to save post-harvest food crops. Annu. Res. Rev. Biol. 16:1-16.
32 Frey-Klett, P., Burlinson, P., Deveau, A., Barret, M., Tarkka, M. and Sarniguet, A. 2011. Bacterial-fungal interactions: hyphens between agricultural, clinical, environmental, and food microbiologists. Microbiol. Mol. Biol. Rev. 75:583-609.   DOI
33 Hanif, A., Zhang, F., Li, P., Li, C., Xu, Y., Zubair, M., Zhang, M., Jia, D., Zhao, X., Liang, J., Majid, T., Yan, J., Farzand, A., Wu, H., Gu, Q. and Gao, X. 2019. Fengycin produced by Bacillus amyloliquefaciens FZB42 inhibits Fusarium graminearum growth and mycotoxins biosynthesis. Toxins 11:295.   DOI
34 Schwyn, B. and Neilands, J. B. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160:47-56.   DOI
35 Shade, A., Jacques, M. A. and Barret, M. 2017. Ecological patterns of seed microbiome diversity, transmission, and assembly. Curr. Opin. Microbiol. 37:15-22.   DOI
36 Sharifazizi, M., Harighi, B. and Sadeghi, A. 2017. Evaluation of biological control of Erwinia amylovora, causal agent of fire blight disease of pear by antagonistic bacteria. Biol. Control 104:28-34.   DOI
37 Sholberg, P., Marchi, A. and Bechard, J. 1995. Biocontrol of postharvest diseases of apple using Bacillus spp. isolated from stored apples. Can. J. Microbiol. 41:247-252.   DOI
38 Spadoni, A., Guidarelli, M., Phillips, J., Mari, M. and Wisniewski, M. 2015. Transcriptional profiling of apple fruit in response to heat treatment: involvement of a defense response during Penicillium expansum infection. Postharvest Biol. Technol. 101:37-48.   DOI
39 Wen, Z., Duan, T., Christensen, M. J. and Nan, Z. 2015. Bacillus subtilis subsp. spizizenii MB29 controls alfalfa root rot caused by Fusarium semitectum. Biocontrol Sci. Technol. 25:898-910.   DOI
40 Wang, Y., Yuan, Y., Liu, B., Zhang, Z. and Yue, T. 2016. Biocontrol activity and patulin-removal effects of Bacillus subtilis, Rhodobacter sphaeroides and Agrobacterium tumefaciens against Penicillium expansum. J. Appl. Microbiol. 121:1384-1393.   DOI
41 Yang, H., Li, X., Li, X., Yu, H. and Shen, Z. 2015. Identification of lipopeptide isoforms by MALDI-TOF-MS/MS based on the simultaneous purification of iturin, fengycin, and surfactin by RP-HPLC. Anal. Bioanal. Chem. 407:2529-2542.   DOI
42 Avalos, S. R., Martinez-Peniche, R. A., Soto-Munoz, L. and Chavaro-Ortiz, M. S. 2012. Modes of action of four strains of antagonistic yeasts against Penicillium expansum LINK in apple. Rev. Chapingo. Ser. Hortic. 18:227-238.   DOI
43 Barad, S., Espeso, E. A., Sherman, A. and Prusky, D. 2016. Ammonia activates pacC and patulin accumulation in an acidic environment during apple colonization by Penicillium expansum. Mol. Plant Pathol. 17:727-740.   DOI
44 Bevardi, M., Frece, J., Mesarek, D., Bosnir, J., Mrvcic, J., Delas, F. and Markov, K. 2013. Antifungal and antipatulin activity of Gluconobacter oxydans isolated from apple surface. Arh. Hig. Rada. Toksikol. 64:279-284.   DOI
45 Wrona, B. and Grabowski, M. 2004. Influence of fructose and glucose occurring on fruit surface on the growth of fungi that cause sooty blotch of apple. J. Plant Prot. Res. 44:287-291.
46 Xu, X. M. and Jeger, M. J. 2013. Combined use of two biocontrol agents with different biocontrol mechanisms most likely results in less than expected efficacy in controlling foliar pathogens under fluctuating conditions: a modeling study. Phytopathology 103:108-116.   DOI
47 Yu, S.-M., Oh, B.-T. and Lee, Y. H. 2012. Biocontrol of green and blue molds in postharvest satsuma mandarin using Bacillus amyloliquefaciens JBC36. Biocontrol Sci. Technol. 22:1181-1197.   DOI
48 Yu, X., Ai, C., Xin, L. and Zhou, G. 2011. The siderophore-producing bacterium, Bacillus subtilis CAS15, has a biocontrol effect on Fusarium wilt and promotes the growth of pepper. Eur. J. Soil Biol. 47:138-145.   DOI
49 Zhang, Y., Li, P. and Cheng, L. 2010. Developmental changes of carbohydrates, organic acids, amino acids, and phenolic compounds in 'Honeycrisp' apple flesh. Food Chem. 123:1013-1018.   DOI
50 Jackson, C. R. and Denney, W. C. 2011. Annual and seasonal variation in the phyllosphere bacterial community associated with leaves of the southern Magnolia (Magnolia grandiflora). Microb. Ecol. 61:113-122.   DOI
51 Janaki, T., Nayak, B. K. and Ganesan, T. 2016. Antifungal activity of soil actinomycetes from the mangrove Avicennia marina. J. Med. Plants Stud. 4:05-08.
52 Janisiewicz, W. 1996. Ecological diversity, niche overlap, and coexistence of antagonists used in developing mixtures for biocontrol of postharvest diseases of apples. Phytopathology 86:473-479.   DOI
53 Janisiewicz, W. J., Jurick, W. M. 2nd, Peter, K. A., Kurtzman, C. P. and Buyer, J. S. 2014. Yeasts associated with plums and their potential for controlling brown rot after harvest. Yeast 31:207-218.   DOI
54 Kaur, A., Sood, A., Kaur, S. and Bhowate, P. 2017. Bacterial population associated with fruits and vegetables and its treatment using antimicrobial rinsing. Int. J. Curr. Microbiol. Appl. Sci. 6:2099-2107.
55 Janssen, B. J., Thodey, K., Schaffer, R. J., Alba, R., Balakrishnan, L., Bishop, R., Bowen, J. H., Crowhurst, R. N., Gleave, A. P., Ledger, S., McArtney, S., Pichler, F. B., Snowden, K. C. and Ward, S. 2008. Global gene expression analysis of apple fruit development from the floral bud to ripe fruit. BMC Plant Biol. 8:16.   DOI
56 Juhnevica, K., Skudra, G. and Skudra, L. 2011. Evaluation of microbiological contamination of apple fruit stored in a modified atmosphere. Environ. Exp. Biol. 9:53-59.
57 Kasfi, K., Taheri, P., Jafarpour, B. and Tarighi, S. 2018. Characterization of antagonistic microorganisms against Aspergillus spp. from grapevine leaf and berry surfaces. J. Plant Pathol. 100:179-190.   DOI
58 Kindt, R. and Code, R. 2005. Tree diversity analysis: a manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre, Nairobi, Kenya. 203 pp.
59 Burch, A. Y., Do, P. T., Sbodio, A., Suslow, T. V. and Lindow, S. E. 2016. High-level culturability of epiphytic bacteria and frequency of biosurfactant producers on leaves. Appl. Environ. Microbiol. 82:5997-6009.   DOI
60 Bever, J. D., Platt, T. G. and Morton, E. R. 2012. Microbial population and community dynamics on plant roots and their feedbacks on plant communities. Annu. Rev. Microbiol. 66:265-283.   DOI
61 Calvo, J., Calvente, V., de Orellano, M. E., Benuzzi, D. and Sanz de Tosetti, M. I. 2007. Biological control of postharvest spoilage caused by Penicillium expansum and Botrytis cinerea in apple by using the bacterium Rahnella aquatilis. Int. J. Food Microbiol. 113:251-257.   DOI
62 Demoz, B. T. and Korsten, L. 2006. Bacillus subtilis attachment, colonization, and survival on avocado flowers and its mode of action on stem-end rot pathogens. Biol. Control 37:68-74.   DOI
63 Calvo, H., Marco, P., Blanco, D., Oria, R. and Venturini, M. E. 2017. Potential of a new strain of Bacillus amyloliquefaciens BUZ-14 as a biocontrol agent of postharvest fruit diseases. Food Microbiol. 63:101-110.   DOI
64 Campos-Martinez, A., Velazquez-del Valle, M. G., Flores-Moctezuma, H. E., Suarez-Rodriguez, R., Ramirez-Trujillo, J. A. and Hernandez-Lauzardo, A. N. 2016. Antagonistic yeasts with potential to control Colletotrichum gloeosporioides (Penz.) Penz. & Sacc. and Colletotrichum acutatum J.H. Simmonds on avocado fruits. Crop Prot. 89:101-104.   DOI
65 Chen, X., Zhang, Y., Fu, X., Li, Y. and Wang, Q. 2016. Isolation and characterization of Bacillus amyloliquefaciens PG12 for the biological control of apple ring rot. Postharvest Biol. Technol. 115:113-121.   DOI
66 de Oliveira Nascimento, I., Rodrigues, A. A. C., Moraes, F. H., de Sousa, F. A., Corsi, M. C. F. and de Moraes Catarino, A. 2016. Isolation, identification and in vitro evaluation of Bacillus spp. in control of Magnaporthe oryzae comparing evaluation methods. Afr. J. Agric. Res. 11:1743-1749.   DOI
67 Nongkhlaw, F. M. and Joshi, S. R. 2015. Investigation on the bioactivity of culturable endophytic and epiphytic bacteria associated with ethnomedicinal plants. J. Infect. Dev. Ctries. 9: 954-961.   DOI
68 Malfanova, N., Kamilova, F., Validov, S., Shcherbakov, A., Chebotar, V., Tikhonovich, I. and Lugtenberg, B. 2011. Characterization of Bacillus subtilis HC8, a novel plant-beneficial endophytic strain from giant hogweed. Microb. Biotechnol. 4:523-532.   DOI
69 Methe, B. A., Hiltbrand, D., Roach, J., Xu, W., Gordon, S. G., Goodner, B. W. and Stapleton, A. E. 2020. Functional gene categories differentiate maize leaf drought-related microbial epiphytic communities. PLoS ONE 15:e0237493.   DOI